Review of resistance to chronic ionizing radiation exposure under environmental conditions in multicellular organisms

Journal of Environmental Radioactivity 212 (2020) 106128

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Review of resistance to chronic ionizing radiation exposure under environmental conditions in multicellular organisms Igor Shuryak Center for Radiological Research, Columbia University Irving Medical Center, 630 West 168th Street, VC-11-234/5, New York, NY, USA

A R T I C L E I N F O

A B S T R A C T

Keywords: Radioactive contamination Radioresistance Chronic irradiation Plants Animals

Ionizing radiation resistance occurs among many phylogenetic groups and its mechanisms remain incompletely understood. Tolerances to acute and chronic irradiation do not always correlate because different mechanisms may be involved. The radioresistance phenomenon becomes even more complex in the field than in the labo­ ratory because the effects of radioactive contamination on natural populations are intertwined with those of other factors, such as bioaccumulation of radionuclides, interspecific competition, seasonal variations in envi­ ronmental conditions, and land use changes due to evacuation of humans from contaminated areas. Previous reviews of studies performed in radioactive sites like the Kyshtym, Chernobyl, and Fukushima accident regions, and of protracted irradiation experiments, often focused on detecting radiation effects at low doses in radio­ sensitive organisms. Here we review the literature with a different purpose: to identify organisms with high tolerance to chronic irradiation under environmental conditions, which maintained abundant populations and/ or outcompeted more radiosensitive species at high dose rates. Taxa for which consistent evidence for radio­ resistance came from multiple studies conducted in different locations and at different times were found among plants (e.g. willow and birch trees, sedges), invertebrate and vertebrate animals (e.g. rotifers, some insects, crustaceans and freshwater fish). These organisms are not specialized “extremophiles”, but tend to tolerate broad ranges of environmental conditions and stresses, have small genomes, reproduce quickly and/or disperse effectively over long distances. Based on these findings, resistance to radioactive contamination can be examined in a more broad context of chronic stress responses.

1. Introduction Ionizing radiation is well known for its lethal, mutagenic and carci­ nogenic effects. The ability of some organisms from various taxonomic groups to resist radiation doses many orders of magnitude above natural levels is an intriguing biological phenomenon that remains incompletely understood (Bruckbauer et al., 2019; Dadachova and Casadevall, 2008; Daly et al., 2004; Gladyshev and Meselson, 2008; Mattimore and Bat­ tista, 1996; Sharma et al., 2017). Importantly, resistance to large radi­ ation doses delivered acutely (over times shorter than those needed for cellular damage repair) often does not translate into resistance to chronic exposures over multiple generations, and vice versa (Kovalchuk et al., 2007; Mitchell et al., 1979; Shuryak et al., 2019, 2017). Such differences between resistances to acute and protracted exposures probably occur because distinct mechanisms and adaptations are required to recover from large amounts of simultaneously generated damage, compared with those needed to deal with a constant rate of damage accumulation.

In addition, radiation tolerance to protracted exposures in the lab­ oratory may not result in resistance to radioactive contamination in the environment (e.g. from nuclear power plant accidents). This can occur because factors like interspecific competition and fluctuations of resource availability and environmental conditions are generally not assessed in laboratory experiments, but are important in the field (Br�echignac et al., 2016; Garnier-Laplace et al., 2013). Synergistic in­ teractions between these factors and radiation can occur. For these reasons, resistance to chronic irradiation under environ­ mental conditions, when entire communities of organisms are exposed over long times (many years/generations), is a relatively under-studied phenomenon. The main sources of information about it (summarized in Table 1) include the following. (1) Radioactive contamination of large areas due to accidents like Kyshtym (Russia), Chernobyl (Ukraine) and Fukushima (Japan), or nuclear waste releases like those from the Mayak plutonium plant in Russia (the location of the Kyshtym accident), or the Oak Ridge facilities in USA (Beresford et al., 2019b; Fesenko, 2018; Pryakhin et al., 2016; Sugiura et al., 2016; Trabalka and Allen, 1977).

E-mail address: [email protected]. https://doi.org/10.1016/j.jenvrad.2019.106128 Received 21 November 2019; Received in revised form 2 December 2019; Accepted 3 December 2019 Available online 6 December 2019 0265-931X/© 2019 Elsevier Ltd. All rights reserved.

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Journal of Environmental Radioactivity 212 (2020) 106128

like large mammals. It enabled them to successfully colonize contami­ nated areas, especially after radiation dose rates dropped from initial peak values due to decay of short-lived radionuclides (Deryabina et al., 2015; Frantsevich, 2006; Fuma et al., 2016; Sokolov et al., 1993; Webster et al., 2016). To reduce the effects of such confounding factors, we focused on identifying those taxa for which the evidence for resistance to chronic radiation exposures came from multiple studies of different radiation types from different times and locations. For example, birch trees (genus Betula) exhibited considerable resistance (especially compared with coniferous trees) to external gamma radiation, based on studies in North America (Amiro and Dugle, 1985; Amiro and Sheppard, 1994), as well as to radionuclide contamination at Chernobyl (Beresford et al., 2019b; Geras’kin et al., 2016) and Kyshtym (Akleyev et al., 2017; Fesenko, 2018). Such consistency of findings across studies suggests that the given taxon is indeed radioresistant relative to its competitors in the investigated communities. Since the number of severely radioactively contaminated sites in the world is (fortunately) limited, and the number of long-term field irra­ diation experiments is limited as well (Table 1), consistent information on radioresistance under environmental conditions is available only for a few taxa of multicellular organisms. Of course, these limitations result in certain selection biases. For example, taxa whose radiosensitivity could be investigated in several studies performed at different times in different locations are likely to be widely distributed and convenient to observe/collect. In contrast, such information is unlikely to be available for species that are endemic, rare and/or difficult to monitor. Despite such limitations, identifying organisms whose populations demonstrated robustness under severe radioactive contamination and/ or protracted experimental irradiation is valuable for enhancing current understanding of chronic radiation resistance. Here we discuss such taxa, which include several terrestrial plants, terrestrial and aquatic invertebrates, and fish. Although the phenomenon of radiation resis­ tance is not fully understood and different mechanisms are likely to be involved to different extents in different organisms, we discuss some plausible potential contributors to this phenotype. They include haploid genome size, because it is well known that genome size and related parameters are inversely correlated with radiation resistance (Sparrow and Miksche, 1961). Also relevant is heavy metal tolerance, because heavy metal toxicity can share some common mechanisms with radia­ tion toxicity such as oxidative stress (Isaksson, 2010; Nuran Ercal et al., 2005; Shuryak et al., 2019). Mentioning these and other factors allows the phenomenon of chronic radiation resistance to be considered in the more general context of stress responses (Cramer et al., 2011; Lushchak, 2011; Wendelaar Bonga, 1997).

Table 1 Main sources of information about resistance to chronic irradiation under environmental conditions reviewed here. We focused on those locations/studies that included high radiation dose rates and/or long durations of exposure. Radiation types and locations, selected references External gamma radiation studies: USA (Flaccus et al., 1974; Olsvig, 1979; Woodwell and Whittaker, 1968) USA (Fraley, 1987) Canada (Amiro and Dugle, 1985; Amiro and Sheppard, 1994; Dugle and Mayoh, 1984) Radioactively contaminated areas: Oak Ridge, USA (Blaylock, 1965; Crossley and Howden, 1961; Plummer and L., 1960; Trabalka and Allen, 1977) Kyshtym accident zone, Russia (Fesenko, 2018; Geras’kin et al., 2016; Sazykina and Kryshev, 2006) Mayak plutonium plant area, Russia ( Pryakhin et al., 2016; Triapitsyna et al., 2012) Chernobyl accident zone, Ukraine ( Beresford et al., 2019b; Bezrukov et al., 2015; Deryabina et al., 2015; Geras’kin et al., 2016; Møller and Mousseau, 2009; Sokolov et al., 1993) Fukushima accident zone, Japan (Fuma et al., 2016; Sugiura et al., 2016; Yoshioka et al., 2015)

Affected areas

Exposure duration

Forest

1961–1976

Grassland Forest

1969–1978 1973–1986

Various (terrestrial and fresh water)

Since 1943

Various (mainly terrestrial)

Since 1957

Fresh water bodies

Since 1949

Various (terrestrial and fresh water)

Since 1986

Various (mainly marine and terrestrial)

Since 2011

(2) Field experiments, where communities of organisms (e.g. forest) were exposed to external gamma radiation (Amiro and Dugle, 1985; Amiro and Sheppard, 1994; Olsvig, 1979; Woodwell and Whittaker, 1968) or to certain radionuclides (Krivolutsky et al., 1992; Styron and Dodson, 1973). Previous reviews of such literature often focused on detecting adverse radiation effects at low contamination levels, e.g. (Andersson et al., 2009; Beresford et al., 2019a; Einor et al., 2016; Møller and Mousseau, 2015; Mothersill et al., 2017; Real and Garnier-Laplace, 2019; Sample et al., 1995; Sazykina et al., 2009). This approach is useful for identifying radiosensitive organisms and for developing guidelines for radiation protection of the environment. In contrast, the phenomenon of resistance to chronic irradiation over multiple years/­ generations, which can also be examined based on the same pool of literature, received much less attention. Here we focused on such resistance, seeking to identify those organisms that were able to main­ tain abundant populations under high radiation levels in the studied community and/or to colonize highly irradiated areas, e.g. due to a competitive advantage over more radiosensitive species. Stable or increasing population sizes under chronic exposure of course do not mean that the studied taxon is unaffected by radiation. Both laboratory and field studies show that the health and lifespan of individuals, their reproductive performance and/or genomic stability can be substantially reduced by radiation, but, as long as these effects are not overwhelming, the population is still able to maintain itself (Kiefer et al., 1975; Marshall, 1966; Polikarpov, 1998). In addition, ra­ diation responses in the field are modulated by multiple factors. For example, radioactive contamination of the environment, e.g. due to the Chernobyl and Fukushima accidents, caused evacuation of humans, thereby weakening many human-imposed pressures and constraints on organisms such as large wild mammals. Before the accidents these species were maintained at low population densities or completely ab­ sent from the area due to hunting by humans and/or land use for agri­ cultural and residential purposes. Land abandonment by humans created potentially suitable habitats, in effect counterbalancing the negative effects of radiation on some generally radiosensitive organisms

2. Terrestrial plants Several experimental studies (Table 1) exposed natural terrestrial communities of organisms to chronic external gamma radiation from a single powerful source over multiple years (Amiro and Dugle, 1985; Amiro and Sheppard, 1994; Flaccus et al., 1974; Olsvig, 1979; Woodwell and Whittaker, 1968). Dose rates decreased with distance from the source, resulting in approximately circular iso-dose rate lines, where a “ring” with a given radius received a given dose rate. Some modulations of the dose rate occurred due to source decay and local shielding by soil, rocks or tree trunks. Overall, however, such experiments provided controlled and relatively uniform external exposure regimes. This point-source study design was not very informative for evalu­ ating radiation effects on highly mobile animals, which did not remain at a fixed distance from the source for long periods, but it did provide valuable information about plants, especially perennial species. Very close to the source, the dose rate could become sufficiently large to exterminate all vegetation (Olsvig, 1979; Woodwell and Whittaker, 1968), although this was not achieved in all studies (Amiro and Shep­ pard, 1994). Somewhat further away, vegetation persisted, but 2

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MBq m 2 for 90Sr was achieved, and changes in the structure of the plant community occurred. Plants with winter seeds disappeared, and there was an initial decline in the cumulative stock of the above-ground biomass by 30%. Up to 5–6 years after the accident, there was a considerable decline in the fraction of plant cover with buds on the soil surface (the obvious result of damage to reproductive organs), and an increase in the proportion of plants with buds within the soil. In the following 5–6 years a slow recovery of the plant community was noticed, although it failed to achieve the pre-accidental state.” Somewhat similar patterns occurred after the Chernobyl accident in 1986, including radiation-induced death of coniferous trees in a heavily contaminated area that became known as the “Red Forest”. Deciduous trees such as birches (genus Betula) proved to be much more tolerant to radioactive pollution compared with conifers (Sokolov et al., 1993). As summarized by (Sokolov et al., 1993), “in birches, where the dosage reached 500 Gy, young apical shoots partially died off, while by mid-August 1986, the foliage was mostly yellow and fell off. By autumn, necrosis of some individual branches was recorded. In the spring of 1987, in many birches at these sites, abundant flowering was recorded, and some of the generative organs of the birch were anomalous in structure. Some male and female catkins branched, and were twisted in shape, and some of the anthers were necrotized. By mid-summer, the majority of birches acquired a peculiar coloration, the central part of the leaf lamina remaining green, while the peripheral portion became bright yellow. In the upper part of the crown, some very large dark-green leaves developed. During 1988, the birches regained their normal fo­ liage.” (Geras’kin, 2016) noted that: “Destruction of the pine canopy greatly changed the microenvironment of the stand, rendering it similar to that of an open field. Since 1988, the Red Forest has been undergoing a community shift that has gradually been replaced by grasses, shrubs, and young deciduous trees. In this radioecological situation radio­ resistant species were actively developing due to an improvement of light, temperature and nutrition conditions. Changes in microclimate and structure of grass communities within the area of died pine stands and severely affected birch stands led to a 3-5-fold increase in biomass of grass. In meadow plant communities near Chernobyl NPP for the same reasons relative contributions of the radioresistant species increased significantly, while the total number of plants and species diversity decreased sharply with the level of radiation exposure.” Compared with external gamma radiation studies, land contamina­ tion with radionuclides from nuclear power plant accidents or weapons production activities (Table 1) produced much more complex irradia­ tion patterns. Some of the reasons for such complexity are described in Table 2. The net consequence of these factors is that the total dose rate from external and internal radiation in a given location can vary by orders of magnitude not only between different species, but also among individuals of the same species (Beresford et al., 2018; Wood et al., 2013). Such variation of dose rates is often better approximated by a log-normal, rather than by a normal, distribution (Beresford et al., 2018; Wood et al., 2013). In these complex situations, physiological radioresistance is not the only determinant of a taxon’s response to radioactive contamination. The following factors can also be important: (1) Low bioaccumulation potential for the dominant radionuclides, due to metabolic specifics of the taxon and/or its lifestyle, as well as local soil composition, can substantially reduce the average radiation dose rate for this taxon, compared with others inhabiting the same location. In essence, a ten­ dency to hyperaccumulate radionuclides can offset physiological radi­ oresistance in some taxa, whereas the opposite tendency can in effect enhance radioresistance in others. (2) A high capacity to invade new habitats can be advantageous because it facilitates colonization of “patches” with low radionuclide deposition and/or locations where dose rates were initially high but subsequently dropped due to short-lived radionuclide decay. Such traits are known to be involved in plant invasiveness in a more general context (Nunez-Mir et al., 2019; �nek, 1996). Rejma

radiosensitive plant taxa became extinct (often within the first year of exposure), and were gradually replaced by more resistant ones. This resulted in changes of vegetation composition as function of distance from the source because distance was correlated with dose rate. For example, in the Canadian FIG study (Amiro and Sheppard, 1994) a devastated zone in the ground vegetation did not occur, and a herb community dominated by Fragaria virginiana, Calium septentrionale, Luzula acurninatn, and Aster spp. survived at dose rates up to 65 mGy/h (65,000 μGy/h). In the US grassland irradiation study (Fraley, 1987), all vegetation was killed only at dose rates >50 R/h (~440,000 μGy/h) and the most resistant perennial species – Gaura coccinea – survived up to 36 R/h (~315,000 μGy/h). Over several years of external irradiation, community changes approached equilibrium, and concentric zones dominated by certain plant species were established. In effect, a specific plant species could achieve dominance in a ring-shaped region where the dose rate was low enough to be tolerated, but high enough to eliminate more radiosensi­ tive competitors. In the US Brookhaven forest studies for example (Flaccus et al., 1974; Olsvig, 1979; Woodwell and Whittaker, 1968), a zone dominated by the sedge Carex pensylvanica was very prominent and persistent between ~20 and 40 m from the source, which corresponded to 126-25 R/day [~46,000–9,000 μGy/h] several years after the start of exposure, in 1973 (Flaccus et al., 1974). “The responses of [other] species to radiation intensity varied. The Rumex population shifted to­ ward the source from 1968 to 1973; it declined in density in the 40–50 m zone and expanded in the 20–40 m zones. In 1973 vigorous individuals of this species were found as close as 18 m from the source (158 R/day) [~58,000 μGy/h]. … There has been a spectacular expansion of the Rubus spp. complex [close to the source] … This expansion was largely clonal, though the presence of some new colonies in 1973 suggests that reproduction from seed was also involved” (Flaccus et al., 1974). In Canadian studies (Dugle and Mayoh, 1984), the resistant plant species in decreasing order of survival at a dose rate >25 mGy/h (25,000 μGy/h) were: “Rubus idaeus, Vaccinium myrlilloides, Ledum groenlandicum, Ribes hirtellum, R. lriste, Salix bebbiana, Ribes glandulosum, Vaccinium angusti­ folium, Rosa spp. (especially the naturally occurring hybrids of Rosa), Salix discolor, Diervilla lonicera, Lonicera dioica, Amelanchier spp., Corylus cornuta, Symphoricarpos albus and Prunus pennsylvanica”. These general findings of changes in plant community composition in multi-year studies were consistent with those of shorter-term studies, e.g. (Zavit­ kovski and Salmonson, 1975). Massive radionuclide releases by the Kyshtym (1957) and Chernobyl (1986) accidents also produced marked changes in plant community composition. As summarized by (Fesenko, 2018) “during the first two years after the [Kyshtym] accident, pine trees died completely within the area with the initial contamination density of 90Sr at a level of 6.0–8.0 MBq m 2, where doses to the needles were in a range of 20–40 Gy and doses to the buds ranged from 10 to 20 Gy. Radiation effects in deciduous forests were observed … where the dose to buds reached 100–200 Gy. The mortality of 50% of deciduous trees was observed at the site with area of around 3 km2, with 90Sr contamination density at about 140 MBq m 2. Thirty percent of trees totally lost their crowns, and 70% of the understory died at that contamination density. Mortality of deciduous trees of around 10% was observed at the area of 12 km2 with initial 90Sr contamination density of 90–100 MBq m 2. The doses to the crowns (bud meristem) at the site were about 100 Gy. Thus, the absor­ bed doses of 100–150 Gy accumulated in the bud meristem induced the partial drying of trees and the death of birch trees was observed at the ‘acute’ dose of 200 Gy. Around 1% of the deciduous trees have lost crowns at the sites with the lower 90Sr contamination density of 37–59 MBq m 2. Such effects were observed within an area of 15 km2 with doses of 40–60 Gy during the first year after the accident. … The most affected pine forest was replaced by either a birch forest or mixed pine-birch forests with dominating birch trees.” Shrubs and herbaceous plants were also affected, as summarized by (Geras’kin, 2016): “In the first vegetation period after the accident contamination density of 37 3

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Table 2 Important reasons for more complicated radiation exposure patterns caused by radioactive contamination (e.g. from nuclear power plant accidents), compared with protracted experimental irradiations. General features

Details

Multiple types of radiation (gamma, beta, alpha) from different radionuclides are involved, vs one type (usually gamma) in experimental exposures. Size of the affected area.

These radiation types have different penetration ranges and relative biological effectiveness (RBE) values.

Complicated temporal pattern of radiation dose rates.

Spatially heterogeneous (“patchy”) radionuclide deposition patterns. Radionuclide bioaccumulation by organisms.

Habitat changes due to radiation effects on other species.

Table 3 Terrestrial plants with high tolerance to chronic irradiation.

Accidentally contaminated areas were often much larger than those used for experimental exposures, and, therefore, more diverse habitats and organisms were affected by radiation. Differences in half-lives of various radionuclides and the rates of transport of radioactive materials throughout the environment (e.g. from tree crowns to the ground) caused dose rates to change over time in a complicated manner. Such spatial heterogeneity occurred due to wind, rainfall, and water drainage patterns and other factors. The chemical properties of specific radionuclides and soil, as well as organism-specific factors, greatly affected the magnitude of radionuclide bioaccumulation and the resulting internal radiation dose rates. Evacuation of humans from contaminated areas had multiple impacts including diminishment of hunting pressures on large mammals and abandonment of agricultural land. Radiation-induced modifications of plant community composition such as replacement of radiosensitive coniferous trees with deciduous ones in heavily contaminated areas also altered the habitat for many other species.

Taxa, genome size, heavy metal tolerance

Location, radiation types

Evidence for radioresistance

Willow trees (genus Salix). Genome size ~425–429 Mb (Dai et al., 2014; Neale et al., 2017). High heavy metal tolerance in some species ( Dos Santos Utmazian et al., 2007; Wang et al., 2014; Zacchini et al., 2011).

External gamma, Canada

Radioresistant, compared with other studied trees. Tolerated dose rates >1,000 μGy/h. Dose rates >13,000 μGy/h had strong negative effects on abundance. Some species tolerated >30,000 μGy/h. Roots received lower dose rates due to shielding ( Amiro and Dugle, 1985; Amiro and Sheppard, 1994; Dugle and Mayoh, 1984). Colonized contaminated areas (Jackson et al., 2005).

Birch trees (genus Betula). Genome size ~430–600 Mb, although some species have >2000 Mb ( Neale et al., 2017; Wang et al., 2016). High heavy metal tolerance in some species (Gussarsson et al., 1996).

Radionuclide contamination, Chernobyl accident zone, Ukraine Radionuclide contamination, Oak Ridge, USA Radionuclide contamination, Fukushima accident zone, Japan External gamma, Canada

Radionuclide contamination, Chernobyl accident zone, Ukraine

In summary, those taxa that strongly accumulate radionuclides, are exposed to highly contaminated substrates, and/or have low mobility have a relative disadvantage in radioactively contaminated areas (Fes­ enko, 2018; Krivolutsky et al., 1992; Krivolutzkii et al., 1992; Sokolov et al., 1993; Zaitsev et al., 2014). These include plants with meristematic tissues located close to the soil surface/organic litter layer and detri­ tivorous soil animals. In contrast, those organisms that combine some degree of physiological radioresistance with high invasiveness/dispersal capacity and low/moderate radionuclide bioaccumulation can gain a competitive edge. Examples of terrestrial plants that appear to have such properties, based on data from external gamma irradiation experiments and from radioactively contaminated sites, are provided in Table 3. Also provided are estimates of the maximum radiation dose rates that these taxa could tolerate, in instances where such numbers were reported in the referenced publications. Dose rate units, which differed between publications, were converted to μGy/h for consistency. The data presented in Table 3 suggest that several deciduous tree taxa such as willows (genus Salix) and birches (genus Betula) were very robust under chronic radiation exposure from external sources and from radioactive contamination in different locations. Although the factors involved in radioresistance of these trees remain to be investigated in detail, the following general observations are likely to be relevant. (1) They are short-lived “pioneer” trees that produce large quantities of seeds, have long seed dispersal distances, exhibit fast juvenile growth, and are common in early successional stages and in disturbed woodlands (Tiebel et al., 2018). (2) They colonize diverse ecological niches such as nutrient-poor, dry, wet, or metal-contaminated environments, and some have high heavy metal tolerance (Dos Santos Utmazian et al., 2007). (3) They have dramatically smaller genome sizes, compared with

Radionuclide contamination, Kyshtym accident zone, Russia

Alder trees (genus Alnus). Genome size 513–983 Mb (Siljak-Yakovlev et al., 2010). High heavy metal tolerance in some species ( Babu et al., 2013; Lee et al., 2009).

External gamma, Canada

Colonized contaminated areas (Crossley and Howden, 1961). Low levels of137Cs bioaccumulation (concentration ratios < 1) (Sugiura et al., 2016). Radioresistant, compared with other studied trees. Tolerated dose rates >1,000 μGy/h. Dose rates >13,000 μGy/h had strong negative effects on abundance. Roots received lower dose rates due to shielding (Amiro and Dugle, 1985; Amiro and Sheppard, 1994; Dugle and Mayoh, 1984). Colonized contaminated areas. Survived doses 10–500 Gy in “acute” phase after the accident (dose rates 6 months later ~2,000–5,000 μGy/h), but with morphological changes and detectable DNA damage (Beresford et al., 2019b; Boubriak et al., 2007; Davids and Tyler, 2003; Geras’kin et al., 2016; Jackson et al., 2005; Kryshev et al., 2005; Sokolov et al., 1993). Radioresistant, compared with other studied trees, to “acute” effects shortly after the accident. Colonized contaminated areas during subsequent years (Fesenko, 2018). Radioresistant, compared with other studied trees. Tolerated dose rates >1,000 μGy/h. However, may be more sensitive than willows (Salix). Dose rates >5,000 μGy/h had strong negative effects on abundance. Roots received lower dose rates due to shielding (Amiro and Dugle, 1985; Amiro and Sheppard, 1994). (continued on next page)

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Table 3 (continued ) Taxa, genome size, heavy metal tolerance

Aspen trees (from genus Populus). Genome size 440–593 Mb (Neale et al., 2017; Siljak-Yakovlev et al., 2010). High heavy metal tolerance in some species (Zacchini et al., � 2011; Zupunski et al., 2016).

Sedges (genus Carex). Genome size ~150–300 Mb, although some species have >1000 Mb ( Lipnerova et al., 2013). Holocentric chromosome structure (Melters et al., 2012) may contribute to radioresistance. High heavy metal tolerance in some species (Matthews et al., 2005; Rofkar and Dwyer, 2011).

Table 3 (continued ) Location, radiation types

Evidence for radioresistance

Radionuclide contamination, Chernobyl accident zone, Ukraine

Colonized contaminated areas. Survived doses 10–100 Gy in “acute” phase after the accident (dose rates 6 months later ~2000–5,000 μGy/h), but with morphologhical changes (Beresford et al., 2019b; Kryshev et al., 2005; Sokolov et al., 1993). Radioresistant, compared with other studied trees. Tolerated dose rates >1,000 μGy/h. Dose rates >11,000 μGy/h had strong negative effects on abundance. Roots received lower dose rates due to shielding (Amiro and Dugle, 1985; Amiro and Sheppard, 1994). Colonized contaminated areas (Sokolov et al., 1993).

External gamma, Canada

Radionuclide contamination, Chernobyl accident zone, Ukraine External gamma, USA

Radionuclide contamination, Chernobyl accident zone, Ukraine Radionuclide contamination, Mayak plutonium plant area, Russia Radionuclide contamination, Oak Ridge, USA

Raspberries and related species (genus Rubus). Genome size 291–308 Mb (Siljak-Yakovlev et al., 2010; VanBuren et al., 2018). 240 Mb (Jung et al., 2019). Low heavy metal bioaccumulation

Radionuclide contamination, Fukushima accident zone, Japan External gamma, Canada

Taxa, genome size, heavy metal tolerance

Location, radiation types

compared with trees ( Wisłocka et al., 2006).

External gamma, USA

Sorrels and related species (genus Rumex). Genome size ~3200–3700 Mb ( Błocka-Wandas et al., 2007; Quesada del Bosque et al., 2011). High heavy metal tolerance in some species (Ban� asov� a et al., 2012; Ye et al., 2012).

Radioresistant, compared with other studied plants. Increased in dominance at high dose rates over time. Tolerated up to ~50,000 μGy/h. Roots received lower dose rates due to shielding (Flaccus et al., 1974; Olsvig, 1979; Woodwell and Whittaker, 1968). Maintained dominance in the zone occupied during irradiation for decades after irradiation (Stalter and Kincaid, 2009). Radioresistant, compared with other studied plants. Had a high density in the radiation zone where most other species were killed ( Fraley, 1987). Compared with other studied plants, Carex accumulated relatively high amounts of137Cs, but low amounts of90Sr ( Kaglyan, 2005). Present on the banks of heavily contaminated water bodies (Pryakhin et al., 2016). Carex and related taxa (Cyperus) colonized contaminated areas ( Crossley and Howden, 1961). Low levels of137Cs bioaccumulation (concentration ratios <1) ( Sugiura et al., 2016). Radioresistant, compared with other studied plants. Increased in dominance at high dose rates over time. Tolerated dose rates >60,000 μGy/h, although numerous somatic mutations were seen on

Radionuclide contamination, Chernobyl accident zone, Ukraine Radionuclide contamination, Fukushima accident zone, Japan External gamma, USA

Radionuclide contamination, Chernobyl accident zone, Ukraine Radionuclide contamination, Fukushima accident zone, Japan

Common reed (Phragmites australis). Genome size ~470–560 Mb (Meyerson et al., 2016). High heavy metal tolerance (Ederli et al., 2004; Hakmaoui et al., 2007).

Radionuclide contamination, Mayak plutonium plant area, Russia Radionuclide contamination, Chernobyl accident zone, Ukraine

Evidence for radioresistance the leaves and flowers produced from overwintering buds on the previous summer’s canes. Roots received lower dose rates due to shielding ( Dugle and Mayoh, 1984). Radioresistant, compared with other studied plants. Increased in dominance at high dose rates over time ( Flaccus et al., 1974; Olsvig, 1979). 137 Cs concentration ratio was ~0.8–8.4, similar to other studied berries ( Yablokov et al., 2011). 137 Cs concentration ratio was <1–6.6, similar to other studied berries ( Sugiura et al., 2016). Radioresistant, compared with other studied plants. Increased in dominance at high dose rates over time. Possible evidence for selection of radioresistant genotypes. Tolerated dose rates up to ~50,000 μGy/ h. Roots received lower dose rates due to shielding (Flaccus et al., 1974; Olsvig, 1979). High LD50 for acute radiation and relatively low bioaccumulation of Cs and Sr, compared with other studied plants ( Gudkov et al., 2011). Generally low levels of137Cs bioaccumulation (concentration ratios <2), although this varied strongly between individuals (Sugiura et al., 2016). Present on the banks of heavily contaminated water bodies (Pryakhin et al., 2016). Present on the banks of heavily contaminated water bodies. However, showed increased chromosomal aberrations and potentially reduced resistance to parasites (mites, fungi) in these areas (Gudkov et al., 2016).

radiosensitive coniferous trees (usually <500 Mb vs. >20,000 Mb), thereby offering smaller “targets” for genotoxic effects of radiation (Neale et al., 2017). These properties probably contribute to the net result that deciduous tree species repeatedly demonstrated high resil­ ience under chronic radiation (Table 3), especially relative to conifers. Tree community responses to severe irradiation may resemble the shifts in dominance from coniferous to deciduous trees after other types of disturbances such as fire (Johnstone et al., 2010). Table 3 also contains evidence for radioresistance of several other plant taxa, such as sedges (genus Carex), raspberries (genus Rubus) and sorrels (genus Rumex). External radiation exposure studies showed that 5

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these plants increased in abundance and even became dominant in highly-irradiated regions close to the source, replacing those taxa that were dominant before irradiation (e.g. forest trees). Studies in radioac­ tively contaminated areas were less informative about the degree of radioresistance of these species because dose rates were generally lower and/or harder to assess. However, these plants remained in contami­ nated locations and/or colonized them, and tended to have low/mod­ erate (rather than high) radionuclide bioaccumulation potential (Table 3). Carex (sedges) is a very large, diverse and widely distributed genus of plants with varied ecology (e.g., they inhabit deserts, tropical forests, tundra) and karyotypes (L�eveill� e-Bourret et al., 2018). Sedges tend to have small genome sizes and holocentric chromosomes, some have high heavy metal tolerance (Table 3). They can achieve dominance in temperate forests subjected to human pressures or fire (Hupperts et al., 2018; Randall and Walters, 2019). Rubus (raspberries) is also a large and diverse genus of plants with small genomes (Table 3) and with variable ploidy levels (Graham and Brennan, 2018). They can quickly take advantage of tree canopy dis­ turbances (e.g. after a fire) due to prodigious fruiting, long-term seed viability and widespread dispersal (Hupperts et al., 2018; Vander Yacht et al., 2017). Because they produce edible berries, radionuclide accu­ mulation in Rubus species was studied extensively in radioactively contaminated areas (Table 3). Rumex (sorrels) is a relatively large and widely-distributed genus as well, with some species being considered weeds. In the Brookhaven forest irradiation experiment, Rumex acetosella increased in dominance at high dose rates over time, along with Carex and Rubus, showing progressive expansion toward the radiation source (Olsvig, 1979). R. acetosella is a common weed that thrives on poor, acidic, and disturbed soils across a broad range of climatic conditions, and its persistent seed bank and vegetative reproduction from creeping roots contribute to its ability to tolerate various stresses including certain herbicides, fire, and tillage (Stopps et al., 2011). Rumex species were also investigated in radioactively contaminated areas, and they tended to have relatively low bioaccumulation potential for dominant radio­ nuclides (Table 3). Interestingly, Rumex genomes are relatively large, similar in size to the human genome (Table 3). The common reed (Phragmites asutralis) is a wetland plant with a worldwide distribution. It was included in Table 3 because there is some evidence for its radioresistance since it persisted in some heavily contaminated water bodies in the Mayak plutonium plant area and the Chernobyl accident region. Radiation-induced damage in this plant was studied in detail in the Chernobyl area, and radiation was potentially involved in increasing reed susceptibility to parasite attacks (Gudkov et al., 2016). The number of plant taxa listed in Table 3 is small because inclusion in the list was based on evidence for radioresistance from multiple chronic radiation studies. In addition, we focused on perennial species because chronic radiation resistance of annual plants is harder to assess based on the literature reviewed here, since individuals derived from seeds brought in from unirradiated areas are exposed to radiation for only one growing season, rather than for multiple years. Only cautious generalization can be made about the properties of this limited number of taxa. It appears that these plants with high tolerance to chronic irradiation tend to have small genomes and demonstrate resilience against various habitat disturbances (e.g. fire) and genotoxic/oxidative stresses including heavy metals.

reproduction, embryonic development and early life stages in general tend to be much more radiosensitive than adults in these organisms, and deleterious transgenerational effects of radiation were also found in several studies (Alonzo et al., 2008; Buisset-Goussen et al., 2014; Lecomte-Pradines et al., 2017; Maremonti et al., 2019; Marshall, 1966; Zaitsev et al., 2014). Consequently, the sensitivity of invertebrate pop­ ulations to chronic irradiation over multiple generations is not as dramatically different from that of vertebrates, as extrapolation based on acute exposures of adults could suggest (Garnier-Laplace et al., 2013). Those invertebrate taxa that inhabit the soil in terrestrial habitats, or bottom sediments in aquatic ones, can be severely affected by radioac­ tive contamination because the contaminants tend to settle in these substrates and result in very high dose rates to local biota (Mietelski et al., 2010; Tikhomirov and Shcheglov, 1994; Zaitsev et al., 2014). Phytophagous taxa may receive lower dose rates due to living at larger distances from contaminated soil/sediments, but they are indirectly affected by radiation-induced changes in plant community composition (Poinsot-Balaguer et al., 1991; Yoshioka et al., 2015). For example, radiation-induced death of radiosensitive coniferous trees in forests where they were dominant before irradiation causes starvation of insects that feed on coniferous trees. More complex indirect effects of radiation can also occur. For example, the survival of gypsy moth caterpillars in the Kyshtym accident area increased (instead of decreasing) with increasing radioactive contamination of the forest because radiation killed an important parasite of these caterpillars – tachinid flies (Ger­ as’kin et al., 2016). The flies were exposed to much higher dose rates than the caterpillars because fly pupae reside in the heavily contami­ nated forest floor, whereas caterpillars and their pupae inhabit the upper tiers of the forest. Evacuation of humans from radioactively contami­ nated areas, which causes dramatic changes in land use patterns and vegetation composition (e.g. gradual conversion of abandoned agricul­ tural land to forests or grasslands), can also have powerful effects on invertebrate communities (Yoshioka et al., 2015). Evidence for resistance to chronic irradiation can be difficult to discern among this multitude of complicating factors. Among aquatic invertebrates, such evidence was found for several taxa that are gener­ ally abundant in fresh water and often serve as model organisms for ecotoxicological studies (Table 4). Rotifers (phylum Rotifera) are the most radioresistant organisms among freshwater zooplankton (Glady­ shev and Meselson, 2008; Pryakhin et al., 2016). This phenomenon was discussed in more detail in previous publications, e.g. (Shuryak, 2019). Planktonic crustaceans (water fleas, order Cladocera) are not as resistant as Rotifera, but they tolerated high dose rates in laboratory studies and some species persisted in very heavily contaminated water bodies in the Mayak plutonium plant region (Table 4). In the Chernobyl accident region, these taxa were studied decades after the accident and no statistically significant radiation effects were detected, probably because dose rates were relatively low at that time (Table 4). Cladocera such as the common genus Daphnia have small genomes and high reproduction rates, which may contribute to resilience under chronic irradiation (Table 4). They are widely distributed and some are model organisms for laboratory research on the effects of radiation and other toxic exposures. As mentioned previously, benthic (bottom-dwelling) invertebrates can be more susceptible to radioactive contamination than planktonic species because radionuclides settle in the sediments, causing highly intense external and internal exposure to benthic fauna. Studies in heavily contaminated water bodies in the Mayak plutonium plant region showed that radionuclide content in silt exceeding ~7.4 � 108 Bq/kg was lethal to all benthic animals, some chironomid larvae and oligo­ chaete worms tolerated somewhat lower levels, and a near-normal benthic species composition persisted below ~1.9 � 107 Bq/kg (Prya­ khin et al., 2016). Mollusks appeared to be the most radiosensitive benthic group, and tolerated only much lower radionuclide contami­ nation levels, below ~7.4 � 104 Bq/kg (Pryakhin et al., 2016).

3. Invertebrate animals Many invertebrate animals exhibit strong radioresistance when acutely irradiated as adults, surviving doses up to 1–3 orders of magnitude above those lethal to mammals (Bakri et al., 2006; Rose, 1992). Some cell lines derived from invertebrates are also highly radi­ oresistant in the laboratory (Sharma et al., 2016). However, 6

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Table 4 Aquatic invertebrate animals with high tolerance to chronic irradiation. Taxa, genome size, heavy metal tolerance

Location, radiation types

Evidence for radioresistance

Phylum Rotifera. Genome size 129.6 Mb for Brachionus calyciflorus ( Kim et al., 2018). Genome size database: ~59–340 Mb. Frequently used in ecotoxicology studies ( Won et al., 2017).

Radionuclide contamination, Mayak plutonium plant area, Russia

Order Cladocera (phylum Arthropoda). Genome size ~200–500 Mb in Daphnia species (Colbourne et al., 2011; Lecher et al., 1995). Genome size database. Radiation-induced DNA damage and oxidative stress are studied extensively (Gomes et al., 2018).

Radionuclide contamination, Mayak plutonium plant area, Russia

Became increasingly dominant among zooplankton in water bodies with increasing levels of radioactive contamination. Dominant species: Brachionus calyciflorus, Brachionus urceus, Hexarthra fennica. ( Pryakhin et al., 2016). Zooplankton dose rate up to ~160,000 μGy/h ( Triapitsyna et al., 2012). Cladocera were found in heavily contaminated water bodies (along with Copepoda and Rotifera), although with reduced species numbers and biomass than in less contaminated water bodies (Pryakhin et al., 2016). Cladocera (Daphnia) were found in contaminated water bodies. No statistically significant radiation effects on reproduction, survival and overall fitness were detected. Dose rates <0.1–180 μGy/h ( Goodman et al., 2019). Maximum dose rates tolerated by Daphnia populations varied depending on experimental design, but were generally >160,000 μGy/h. Reproduction was affected at lower dose rates than mortality. Transgenerational effects were reported. (Alonzo et al., 2008, 2006; Gilbin et al., 2008; Marshall, 1966, 1962; Parisot et al., 2015; Turner, 1975). Medium-high137Cs bioaccumulation (concentration ratios >10–100) (Adam et al., 2001; King, 1964). Chironomid larvae dominated zoobethos in a severely contaminated water body where no other benthic animals could survive. Dose rate up to ~46,000 μGy/h (Pryakhin et al., 2016; Triapitsyna et al., 2012). Chironomid larvae were found in contaminated water bodies. Evidence of radiation-induced chromosomal aberrations was reported (Blaylock, 1965).

Radionuclide contamination, Chernobyl accident zone, Ukraine

External gamma or internal alpha, laboratory

Family Chironomidae (phylum Athropoda). Genome size ~117–244 Mb, ~200 Mb in Chironomus tentans ( Kutsenko et al., 2014), genome size database. Known for resistance to large acute radiation doses, perhaps as a byproduct of desiccation tolerance, e.g. (Datkhile et al., 2015). Used in ecotoxicology studies, tolerant to some heavy metals (Park, 2011; Pedrosa et al., 2017). Family Naididae (phylum Annelida). Genome size ~760–7470 Mb, ~3370

Radionuclide contamination, Mayak plutonium plant area, Russia

Radionuclide contamination, Oak Ridge, USA

Radionuclide contamination,

Table 4 (continued ) Taxa, genome size, heavy metal tolerance Mb for Tubifex tubifex ( Gregory and Hebert, 2002). Used in ecotoxicology studies, tolerant to some heavy metals (Vidal and Horne, 2009).

Asellus aquaticus (phylum Arthropoda). Genome size ~1900 Mb (Voolstra et al., 2017). Considered a potential biomonitor of metal pollution due to high tolerance ( O’Callaghan et al., 2019).

Location, radiation types

Evidence for radioresistance

Mayak plutonium plant area, Russia

water bodies, Naididae were reported to be among the most resistant taxa to radioactive contamination (Pryakhin et al., 2016). Three species (Dero obtusa, Nais pseudobtusa and N. pardalis) were studied. Dose rates 0.7–14 μGy/h. Findings: increased chromosomal aberrations in all three species; stimulation of sexual reproduction in some species that usually reproduce asexually ( Tsytsugina and Polikarpov, 2003). Found in contaminated water bodies. No statistically significant radiation effects on reproduction, development and morphology were detected. Dose rates up to 27.1 μGy/h (Fuller et al., 2019, 2018, 2017).

Radionuclide contamination, Chernobyl accident zone, Ukraine

Radionuclide contamination, Chernobyl accident zone, Ukraine

Chironomidae (non-biting midges) is a family of flies (Diptera) with aquatic larvae and pupae. They have a worldwide distribution and often dominate aquatic insect communities in both abundance and species richness (Ferrington, 2008). They have small genomes, and some species tolerate severe stresses, e.g. desiccation, a wide temperature range, low oxygen concentrations, large acute radiation doses, or heavy metals (Table 4). Chironomidae were the most radioresistant among benthic invertebrates in water bodies polluted by the Mayak plutonium plant. As summarized by (Pryakhin et al., 2016), “in reservoir R-17 [which had the second highest radioactive contamination level among the studied water bodies] benthos communities consist only of chironomids. Here chironomids reach the highest abundance among the storage-reservoirs … Zoobenthos biomass is mainly determined by large-size chironomids Psectrotanypus sibiricus.” Freshwater oligochaete worms (family Naididae) also form an important component of benthic fauna throughout the world. Along with Chironomidae, they are often used as model organisms for pollutant toxicity assessments (Lobo and Espindola, 2014). Evidence for resistance to chronic irradiation, as well as indications of radiation-induced dam­ age, are available for both Chironomidae and Naididae from multiple studies (Table 4). Asellus aquaticus is a benthic crustacean from the order Isopoda, which has a wide distribution and is also often used in studies of pollutant effects (O’Callaghan et al., 2019). Its genome is relatively large (much larger than that of planktonic Cladocera such as Daphnia, Table 4) and its radiosensitivity was (to our knowledge) never extensively stud­ ied in the laboratory. Investigations of radioactive contamination effects on A. aquaticus in the Chernobyl accident zone decades after the acci­ dent revealed no statistically significant effects on reproduction, development and morphology, which suggests some degree of radio­ resistance (Table 4). However, dose rates were relatively low at the time of the studies, and an approximately contemporaneous investigation of aquatic macroinvertebrate communities in lakes exposed to Chernobyl-derived radiation reported that no evidence was found in this study that the ecological status of lake communities has been influenced by radioactive contamination from the Chernobyl accident (Murphy et al., 2011). There are multiple studies of chronic radiation effects on terrestrial

Among benthic animals that spend their entire life cycle in contaminated

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invertebrates, where dramatic negative effects of radioactive contami­ nation were reported shortly after a nuclear accident (Krivolutzkii et al., 1992; Sokolov et al., 1993; Tikhomirov and Shcheglov, 1994) or even decades later (Møller and Mousseau, 2009). Taxa that inhabit the topsoil and organic litter and have slow dispersal (e.g. flightless arthropods) tend to be affected most strongly by radioactive fallout, and tend to recover very slowly even when dose rates are reduced. However, some evidence of radioresistance among such soil invertebrates was found for round worms (phylum Nematoda). A study in the Chernobyl accident zone found only subtle effects of radiation 25 years after the accident, suggesting that many nematode species recovered by this time and/or were not severely affected by the accident (Table 5). Ants (family Formicidae) also spend much of their lives in and on the soil, but studies in radioactively contaminated areas tended to show no suppression of their abundance or even an increase in abundance as function of contamination level (Table 5). These findings may be caused by difficulties in accounting for the effects of confounding factors such as changes in habitat due to radiation effects on plants and human evac­ uation. However, the rapid dispersal ability of ants by their flying males

and females probably contribute to their robustness in contaminated areas: ants could quickly colonize suitable areas when dose rates were reduced there by the decay of short-lived radionuclides. Ants also have small genome sizes relative to some other insect orders, which may contribute to radioresistance (Table 5), although their resistance to acute irradiation is not exceptionally high by insect standards (Follett and Taniguchi, 2007). 4. Vertebrate animals Vertebrate animals are generally considered to be a radiosensitive group, with possible contributing factors being large genome sizes and potential for radiation-induced carcinogenesis (which, by comparison, does not appear to be a problem in plants) (Waterworth et al., 2011). Small mammals such as rodents (order Rodentia) represent convenient model organisms for experimental and observational studies. Conse­ quently, numerous studies investigated chronic radiation effects on small mammals in the laboratory (Brown, 1964; French and Kaaz, 1968; Russell et al., 1959; Searle et al., 1980; Sugahara, 1964), in the field using external irradiation sources (French et al., 1974; Mihok, 2004; Turner and Iverson, 1976), and in radioactively contaminated areas (Childs and Cosgrove, 1966; Dunaway and Kaye, 1964; Gaschak et al., 2011b; Jernfors et al., 2018; Kubota et al., 2015; Malinovsky et al., 2014; Mappes et al., 2019; Mustonen et al., 2018; Orekhova et al., 2019; Ryabokon et al., 2005; Ryabokon and Goncharova, 2006; Yalkovskaya et al., 2011). Multiple detrimental radiation effects on reproduction, survival, health status, genomic stability, embryonic mortality, and other endpoints were reported. Transgenerational detrimental effects were detected in the laboratory and probably also occurred in areas contaminated by nuclear accidents (Grigorkina and Olenev, 2012; Ryabokon et al., 2005; Ryabokon and Goncharova, 2006). Some studies suggest that some terrestrial birds and reptiles can be very sensitive to �n et al., 2011; Møller et al., 2012; Møller and chronic irradiation (Galva Mousseau, 2007; Turner et al., 1969; Turner and Medica, 1977). Notably, there are large differences in radiosensitivity between ro­ dent species. For example, murids (e.g., Mus and Rattus spp.) are rela­ tively resistant to chronic irradiation, hystricomorphs (Chinchilla laniger, Cavia porcellus) are extremely sensitive, and one sciurid (Tamias striatus) is highly resistant (Turner, 1975). Also, as discussed above, the effects of radioactive contamination under field conditions are determined not only by intrinsic physiological radiosensitivity, but also by many other factors (Table 2). The complex interactions of these factors resulted in persistence or even increase of the populations of many terrestrial mammal species in radioactively contaminated areas, particularly after dose rates were dramatically reduced by decay of short-lived radionu­ clides in the first few months-years after the start of exposure (Kryshev et al., 2005; Sazykina and Kryshev, 2006; Sokolov et al., 1993). For example, wild boars (Sus scrofa) increased in numbers in areas contaminated by the Chernobyl and Fukushima nuclear power plant accidents (Deryabina et al., 2015; Fuma et al., 2016; Sokolov et al., 1993). Wolves (Canis lupus) are now abundant in the Chernobyl accident area (Byrne et al., 2018; Deryabina et al., 2015), and brown bears (Ursus arctos) are invading it (Gashchak et al., 2016), whereas both species were rare/not present there before the accident. However, none of these species are likely to exhibit particular radioresistance above the average level for mammals. Among aquatic vertebrates (freshwater fish) there is stronger evi­ dence for radioresistance among some species. For example (Fesenko, 2018), reported that: “observations of the carp population of Lake Urus-Kul, exposed to radiation [from the Mayak plutonium plant] over 16 generations, did not show statistically significant differences in the rate of chromosome aberrations compared to a similar uncontaminated lake. Thus, for dose rates to the gonad of 5.0 mGy d 1 [~200 μGy/h] (reported doses to spawn were 1–2 mGy d 1 [~40–80 μGy/h]) the yield of chromosome aberrations was measured to be as low as 2.5%. This value was a bit lower than that observed in the control site of 3.3%.

Table 5 Terrestrial invertebrate animals with high tolerance to chronic irradiation. Taxa, genome size, heavy metal tolerance

Location, radiation types

Evidence for radioresistance

Soil nematodes (phylum Nematoda). Genome size ~70–190 Mb (Fierst et al., 2015), genome size database. Radiation-induced DNA damage and other effects, and heavy metal toxicity, are studied extensively in the model species Caenorhabditis elegans ( Buisset-Goussen et al., 2014; Maremonti et al., 2019; Martinez-Finley and Aschner, 2011). Ants (family Formicidae, phylum Arthropoda). Genome size ~300–400 Mb (Tsutsui et al., 2008). Bioaccumulate heavy metals, but have relatively high tolerance (Grze�s, 2010; Migula et al., 1997).

Radionuclide contamination, Chernobyl accident zone, Ukraine

Slight radiation impacts on soil nematode communities studied 25 years after the accident were reported. No effects on total abundance. Results suggest a possible tolerance of the Leptonchidae family to radiological contamination at studied levels. Dose rates up to 220 μGy/h ( Lecomte-Pradines et al., 2014). Strong positive association between abundance and background radiation dose rate was found for ants from genus Formica ( Bezrukov et al., 2015). Winged ants and workers of Camponotus japonicus and Formica japonica increased in numbers in contaminated areas, potentially due to evacuation of humans ( Yoshioka et al., 2015). 137 Cs activity concentrations in ants were very variable, sometimes very high (~1.5 MBq/kg) in severely contaminated areas, other times low.90Sr and Pu isotope levels were on average 1–3 orders of magnitude lower than137Cs. Concentration ratios values were generally similar to those for vegetation and small mammals (Dragovi�c and Mandi�c, 2010; Gaschak et al., 2011a; Mietelski et al., 2010; Ros�en et al., 2018).

Radionuclide contamination, Chernobyl accident zone, Ukraine

Radionuclide contamination, Fukushima accident zone, Japan

Radionuclide contamination, Chernobyl accident zone, Ukraine, and Chernobyl contaminants in other countries

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Similar effects were observed for the golden carp population sampled in Lake Berdenish. Overall, variabilities in 14 morphometric parameters in crucian carp from lakes Urus-Kul and Berdenish were found not to be statistically different from those in similar lakes located outside the EURT.” In severely contaminated water bodies (Pryakhin et al., 2016), noted that “the following fish species were registered: roach Rutilus rutilus L., tench Tinca tinca L., crucian carp Carassius сarassius L., ide Leuciscus idus L., perch Perca fluviatilis L., pike Esox lucius L. In the catches from reservoir R-3, which freezes from top to the bottom, and demonstrates the presence of fish kill phenomena in winter, only roach and perch were found. In [the most contaminated] reservoirs R-17 and R-9 fish is absent.” In North America, evidence for resistance to radioactive contami­ nation was found for the mosquitofish (Gambusia affinis) (Table 6). It is a small and resilient fish species native to the United States and intro­ duced to many other parts of the world (Pyke, 2005). It was able to maintain abundant populations under high levels of radioactive contamination in the Oak Ridge plant region (Table 6). These results are consistent with general observations that mosquitofish populations can tolerate, and often thrive within, a wide range of conditions (Pyke, 2005). Comparable levels of resistance to radioactive contamination occurred in larger fish species – roach (Rutilus rutilus) and perch (Perca fluviatilis), based on data from the Mayak plutonium plant and Cher­ nobyl areas (Table 6). These fish are widely distributed and are often found together in the same water bodies. Young perch feed on plankton but switch to larger prey, including other fish, as adults, whereas roach are omnivorous throughout their life (Nurminen et al., 2010). Both species maintained abundant populations in freshwater bodies heavily contaminated with radionuclides. There they tolerated dose rates that are quite high for vertebrates (>10 μGy/h) over multiple generations (Table 6).

5. Conclusions Resistance to chronic ionizing radiation exposure is not unique to a specific phylogenetic group, but occurs among all domains of life. This phenotype probably evolved in those organisms whose lifestyle neces­ sitates surviving severe genotoxic and oxidative stresses (e.g. UV radia­ tion, desiccation, toxic chemicals) in their natural environment (Daly et al., 2010; Fredrickson et al., 2008; Krisko et al., 2012; Shuryak, 2019). Here we discussed examples of plants, invertebrate and vertebrate ani­ mals, for which there is considerable evidence of resistance to chronic irradiation under environmental conditions from multiple studies con­ ducted in different locations and at different times, and involving different radiation types. The radiation exposures tolerated by these organisms occurred over many years (which corresponds to multiple generations for many of these species). Importantly, they occurred in the presence of multiple modulating factors such as interspecific competi­ tion and temporal variations in environmental parameters and resource availability. The number of taxa for which consistent evidence of high tolerance to chronic irradiation under field conditions could be found is limited. Also, as mentioned previously, rare and difficult to study species were unlikely to be identified based on the studies reviewed here. However, some general properties shared by many of these taxa can be mentioned (Table 7). These radioresistant multicellular organisms were not specialized “extremophiles”. Instead, they are common species that tolerate wide ranges of environmental conditions and various stressors. This pattern in similar to the one found in microorganisms (Shuryak, 2019). Consequently, resistance to radioactive contamination can be examined in a more broad context of chronic stress responses (Cramer et al., 2011; Lushchak, 2011; Wendelaar Bonga, 1997). Although ionizing radiation is a unique toxic agent in many respects, for example because it produces a wide diversity of damage types to DNA and other macromolecules, often with spatial clustering, there may be substantial overlap between responses to radiation and other stressors like heavy metals (Lushchak, 2011; Shuryak et al., 2019). When a large area is contaminated with radionuclides, examples of organisms that show high tolerance to such contamination are likely to be found among those taxa that are already present in this region and have intrinsic resilience

Table 6 Freshwater fish with high tolerance to chronic irradiation. Taxa, genome size, heavy metal tolerance

Location, radiation types

Evidence for radioresistance

Mosquitofish (Gambusia affinis). Genome size ~700–900 Mb (genome size database), ~683–759 Mb ( Hoffberg et al., 2018). Heavy metal toxicity was studied (Authman, 2015). Roach (Rutilus rutilus), perch (Perca fluviatilis). Genome size ~1000–1800 Mb for Cyprinidae, (Kuang et al., 2016). ~970–1510 Mb for roach (genome size database). ~1000 Mb for perch (Ozerov et al., 2018). Can accumulate heavy metals (Andres et al., 2000; Carru et al., 1996).

Radionuclide contamination, Oak Ridge, USA

Found in contaminated water bodies. Dose rates up to ~25–145 μGy/h ( Blaylock, 1969; Trabalka and Allen, 1977).

Radionuclide contamination, Mayak plutonium plant area, Russia

Radionuclide contamination, Chernobyl accident zone, Ukraine

Table 7 Some general properties of organisms resistant to chronic irradiation from radioactive contamination. Properties

Resulting advantages

Small genome size

Small genomes offer smaller “targets” for toxic effects of radiation such as DNA double strand breaks. There is overlap between adaptations and mechanisms needed to resist chronic irradiation and other genotoxic and oxidative stressors. Taxa that efficiently disperse over long distances (e.g. plants with small seeds carried by wind or animals, flying insects, large mammals) can quickly colonize contaminated areas once dose rates are reduced by decay of short-lived radionuclides. A tendency to hyperaccumulate radionuclides (e. g. cesium, strontium or plutonium isotopes) can result in high internal dose rates, whereas low radionuclide bioaccumulation reduces these dose rates. Radionuclides tend to settle in the topsoil/organic litter layers of terrestrial habitats and in bottom sediments in water bodies. Organisms that spend less time in/on these substrates can receive lower dose rates than those that inhabit them (e.g. pelagic vs benthic aquatic animals). A high reproduction rate can help to compensate for radiation-induced reductions in individual health, life span and fecundity.

Tolerance to multiple stressors

Both species were found in severely contaminated water bodies, where other fish species were absent ( Pryakhin et al., 2016). Dose rate for roach varied between ~30 and 790 μGy/h (Triapitsyna et al., 2012). Both fish species reported to be in good general physiological and reproductive health in studied contaminated water bodies. Perch appeared to be more sensitive to radiation than roach. Total dose rates in 2015 reached 14.1 μGy/h for roach and 15.7 μGy/h for perch (Lerebours et al., 2018).

Long-distance dispersal

Low radionuclide bioaccumulation

Life style that reduces radiation exposure intensity

Rapid reproduction

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against multiple types of stressors. In this review, we focused on finding examples of organisms whose populations tolerated intense chronic irradiation from external sources and/or radioactive contamination of the environment. Investigation of how chronic irradiation affects the genomes an epigenomes of these populations, and their evolution, is an important area for further research (Esnault et al., 2010). Selection of radioresistant lineages (Flaccus et al., 1974; Olsvig, 1979) and radiation adaptive responses may take place (Kovalchuk et al., 2004) under chronic exposure, with epigenetic changes being potentially involved (Boyko and Kovalchuk, 2011). However, evidence for such processes could be detected only in some, but not in all, studied species (Boubriak et al., 2016; Geras’kin et al., 2013; Møller and Mousseau, 2016). For example, mutation fre­ quencies and other radiation damage endpoints in the Chernobyl acci­ dent area decreased as dose rates decreased over time in Arabidopsis thaliana plants (Abramov et al., 1992), but did not decrease or even increased in rodents (Ryabokon et al., 2005; Ryabokon and Goncharova, 2006). Such data suggest that organisms can differ dramatically in resistance not only to radiation-induced mortality and reproductive impairment, but also to genomic instability and other transgenerational effects. Future research is needed to elucidate the chronic radiation resis­ tance phenotype, which probably emerged independently in many phylogenetically distant groups as a byproduct of resistance to other environmentally relevant stressors such as heavy metals, desiccation, ultraviolet light exposure, and elevated temperature. Specifically, it is important to investigate the molecular mechanisms of this phenotype, and the mechanistic overlap between resistances to chronic radiation and some of these other stressors. The rapidly growing fields of systems biology and “omics” sciences (genomics, transcriptomics, proteomics and metabolomics) should have powerful potential in this area. Some of the plant and animal taxa identified here as resistant to radioactive contamination and chronic external irradiation could be used as model organisms for such studies.

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